Prevalence of staphylococcal toxin in food contaminated by Staphylococcus spp.: Protocol for a systematic review with meta-analysis

Background Food contamination by Staphylococcus spp. enterotoxigenic strains is quite common and despite underreporting caused by the short duration of clinical symptoms and lack of medical care, staphylococcal food poisoning is one of the most common Foodborne Diseases (FBD) in the world. This study describes a systematic review protocol with meta-analysis on the prevalence and types of staphylococcal enterotoxins in food, and the profile of contaminated foods. Methods The research will be conducted through the selection of studies reporting the analysis of staphylococcal enterotoxins in food contaminated by Staphylococcus spp. Searches will happen on the following databases: Medline (OVID), GALE, Science Direct, CAB Direct (CABI), Google Scholar, in addition to manual search in the list of references of articles, directory of theses and dissertations, and countries’ health agencies. Reports will be imported into the application Rayyan. Two researchers will independently select studies and extract data, and a third reviewer will solve conflicting decisions. The primary outcome will be the identification of staphylococcal enterotoxins in food, and the secondary outcomes will include staphylococcal enterotoxin types and foods involved. To assess the risk of bias in the studies, the tool developed by the Joanna Briggs Institute (JBI) will be used. For data synthesis, a meta-analysis will be performed. However, in case that is not possible, a narrative synthesis of the most relevant results will be carried out. Discussion This protocol will serve as the basis for a systematic review that aims to relate the results of existing studies on the staphylococcal enterotoxin prevalence and types in food, and the profile of the contaminated foods. The results will broaden the perception of food safety risks, highlight existing literature gaps, contribute to the study of the epidemiological profile and may guide the allocation of health resources for the development of preventive measures related. Systematic review registration PROSPERO registration number: CRD42021258223.

This question relies upon knowledge of the broader characteristics of the population of interest and the geographical area. If the study is of women with breast cancer, knowledge of at least the characteristics, demographics and medical history is needed.
The term "target population" should not be taken to infer every individual from everywhere or with similar disease or exposure characteristics. Instead, give consideration to specific population characteristics in the study, including age range, gender, morbidities, medications, and other potentially influential factors.
For example, a sample frame may not be appropriate to address the target population if a certain group has been used (such as those working for one organization, or one profession) and the results then inferred to the target population (i.e. working adults).
A sample frame may be appropriate when it includes almost all the members of the target population (i.e. a census, or a complete list of participants or complete registry data).
Was the sample used appropriate for the purpose of the study, considering the type of food and the location where it was collected?
-Nature of the samples (Type of food, was the sample part of suspectedly contaminated food?) -City, country of origin, and collection site YES: When the following is specified: • Type of food; • Reason for analyzing the food (e.g., potential outbreak) • Collection site (city, country)

NO:
When the collected sample is not a suspectedly contaminated food or no adequate reason for its inclusion is described in the study (e.g., the food linked to the outbreak is not recovered and other food is analyzed).

UNCLEAR:
When any aspect is unclear or when information is not provided.

2.
Were study participants sampled in an appropriate way?
Studies may report random sampling from a population, and the methods section should report how sampling was performed. Random probabilistic sampling from a defined subset of the population (sample frame) should be employed in most cases, however, random probabilistic sampling is not needed when everyone in the sampling frame will be included/analysed.
For example, reporting on all the data from a good census is appropriate as a good census will identify everybody. When using cluster sampling, such as a random sample of villages within a region, the methods need to be clearly stated as the precision of the final prevalence estimate incorporates the clustering effect. Convenience samples, such as a street survey or interviewing lots of people at public gatherings are not considered to provide a representative sample of the base population.
Were the sampling process and collection method described? Was the study (results / discussion / conclusion) conducted in a coherent way?
Expected description: • Transport at refrigeration temperature and using isothermal boxes • No longer than 36 hours from collection to analysis YES: Information available and adequate.

NO: Information available and inadequate.
UNCLEAR: Information unavailable or inappropriately described, leading to doubts.

3.
Was the sample size adequate?
The larger the sample, the narrower will be the confidence interval around the prevalence estimate, making the results more precise.
An adequate sample size is important to ensure good precision of the final estimate. Ideally we are looking for evidence that the authors conducted a sample size calculation to determine an NOT APPLICABLE.
Question excluded since a positive result for enterotoxin from at least one food sample would be enough to evaluate the study.
adequate sample size. This will estimate how many subjects are needed to produce a reliable estimate of the measure(s) of interest.
For conditions with a low prevalence, a larger sample size is needed. Also consider sample sizes for subgroup (or characteristics) analyses, and whether these are appropriate. Sometimes, the study will be large enough (as in large national surveys) whereby a sample size calculation is not required. In these cases, sample size can be considered adequate.
When there is no sample size calculation and it is not a large national survey, the reviewers may consider conducting their own sample size analysis using the following formula: (Naing et al. 2006, Daniel 1999  Were the study subjects and the setting described in detail? Certain diseases or conditions vary in prevalence across different geographic regions and populations (e. g. Women vs. Men, sociodemographic variables between countries).
The study sample should be described in sufficient detail so that other researchers can determine if it is comparable to the population of interest to them.

Are the different ways of samples treatment described according to the type of food?
YES: There were no differences in sample treatment. OR Differences in methodology were described according to the type of food.
NO: Samples were not treated properly.

UNCLEAR:
The authors did not describe how the different samples were treated. Relevant details were not available.

5.
Was the data analysis conducted with sufficient coverage of the identified sample?
Coverage bias can occur when not all subgroups of the identified sample respond at the same rate.
For instance, you may have a very high response rate overall for your study, but the response rate for a certain subgroup (i.e. older adults) may be quite low.
If there are different subgroups of foods, was a similar number of samples analyzed in all of them?

YES:
• There is no difference in the number of samples between subgroups/types and between methodology and results • The reasons are described for differences, if any, in the number of samples identified and analyzed or differences in sample number between subgroups/types of food NO: When a difference is noticed in the number of samples mentioned in the methodology and in the result section and reasons for so are not listed UNCLEAR: Information unavailable or inappropriately described, leading to doubts. 6.
Were valid methods used for the identification of the condition?
Here we are looking for measurement or classification bias.
Many health problems are not easily diagnosed or defined and some measures may not be capable of including or excluding appropriate levels or stages of the health problem.
If the outcomes were assessed based on existing definitions or diagnostic criteria, then the answer to this question is likely to be yes.
If the outcomes were assessed using observer reported, or selfreported scales, the risk of over-or under-reporting is increased, and objectivity is compromised.
Importantly, determine if the measurement tools used were validated instruments as this has a significant impact on outcome assessment validity

Were valid methods used for toxin determination?
Examples of valid methods: Considerable judgment is required to determine the presence of some health outcomes.
Having established the validity of the outcome measurement instrument (see item 6 of this scale), it is important to establish how the measurement was conducted.
Was the condition measured in the same way for all samples or was there justification for adaptations made? YES: When the following was described and adequate: • sample collection.
• preparation of standard solutions.
• equipment used and whether it is calibrated.
Were those involved in collecting data trained or educated in the use of the instrument/s? If there was more than one data collector, were they similar in terms of level of education, clinical or research experience, or level of responsibility in the piece of research being appraised?
When there was more than one observer or collector, was there comparison of results from across the observers? Was the condition measured in the same way for all participants?
• calculations to determine the results.
-Were the limits of detection (LD) and limits of quantification (LQ) the same in the analysis of different samples of the same food?
NO: When information is available, but inadequate.

8.
Was there appropriate statistical analysis?
Importantly, the numerator and denominator should be clearly reported, and percentages should be given with confidence intervals.
The methods section should be detailed enough for reviewers to identify the analytical technique used and how specific variables were measured.